Nuptial Coloration Research Articles

Does part reproductive history predict competitive interactions and male mating success in pupfish?

Two experiments were performed to determine the effect of past territoriality and mating success on subsequent dominance and ability to attract females. First, in 14 staged, pair-wise encounters, the development of nuptial coloration and agonistic behaviour was examined in two types of males: previously territorial (PT) and previously non-territorial (PNT) males. Previously territorial males developed a more intense nuptial coloration and won all contests. Second, to test the males' ability to attract females, other factors were controlled that could have affected female mate choice, such as male size, quality of breeding substrate and male-male interactions. In 40 trials, PT males were more active, developed a more intense nuptial coloration, courted females more vigorously, spawned sooner and had a higher mating success than PNT males. Thus, in pupfish, Cyprinodon pecosensis, previous reproductive history is a good indicator of both dominance and mating success. Only males in good physical condition achieve high mating success, and both intra- and inter-sexual selection are important in maintaining the close correlation between expression of nuptial coloration, a second sexual trait, and other male attributes, such as physical condition and vigour, that allow a male to secure and defend a territory against rivals and to attract and spawn with females.

Factors Associated With and Fitness Effects of Nest-Raiding in the Three-Spined Stickleback, Gasterosteus Aculeatus, in a Natural Situation

The occurrence and consequences of nest-raiding behaviours of male three-spined sticklebacks (Gasterosteus aculeatus L., forma leiura) were studied in an enclosed section of a small stream of the Tsuya River, Gifu Prefecture Central Japan. The observations were made almost daily on 99 males which were individually marked and the 189 nests built by them during the breeding season, March to mid July 1988. About 10% of the nests were subjected to raiding which included egg cannibalism, egg stealing and sneaking fertilizations. Most raidings were done by single territorial males. The probability of nest raiding was related to the degree of cover around the nest: nests in dense vegetation were most prone to raiders. The probability of raiding was further related to the stage of the nest: nests with eggs were most liable, those with fry least liable to raiding actions. Males that performed raiding behaviour could have nests in every stage, but most likely had no eggs in their nests. The probability of being raided was thus positively related to the number of neighbouring nests without eggs. Males that raided had a significantly duller overall nuptial coloration during the egg collecting phase than non-raiders. Body size and territory size did not differ between raiders and non-raiders. Raiders may thus be less attractive to ripe females. By egg stealing they may increase the attractiveness of their otherwise empty nest to spawning. Indeed, nests of raiders produced significantly more often young than those of non-raiders, but the number of young produced in successful nests was not different between the two categories of males. Nest-raiding was detrimental to the victims of raiding actions: raided nests produced less offspring early in the breeding season.

Nuptial Colour Loss and Signal Masking in Gasterosteus: an Analysis Using Video Imaging

Threespine stickleback vary greatly in male nuptial display, from full red expression between the throat and pelvis to total melanism without any traces of red. The dominant expression for any population is correlated with the underwater spectral irradiance and many populations with melanistic nuptial colour occur in bog habitats where the aquatic spectrum is shifted to long wavelengths. Field observations indicate that in these bog habitats, the typical red nuptial signal is 'spectrally masked' and this might reduce the effectiveness of display during male-male and male-female interactions. We used video imaging techniques to test whether the spectral composition of the visual background influences female preference for nuptial colouration in male threespine sticklebacks. Throat colour preference tests were carried out in which females chose between video images of red and black-throated males superimposed on either a blue or a red background. Despite belonging to a red-throated population, females were found to respond preferentially to the black-throated male image viewed against a red background, indicating that preference was not determined by throat patch hue. This suggests that preference for an epigamic optical signal is likely a function of its efficacy in generating visual contrast rather than its intrinsic spectral characteristics.

The Mechanisms of Colour-Based Mate Choice in Female Threespine Sticklebacks: Hue, Contrast and Configurational Cues

We investigated the importance of male nuptial colouration as a cue for female mate choice in the threespine stickleback Gasterosteus aculeatus L. In courtship preference tests, sexually receptive females were presented with pairs of dummies that differed in the hue, extent or distribution of colouration. Females preferred to court i) a red-bellied dummy over a green-bellied dummy, a uniformly tan dummy, and an all-red dummy and ii) a yellow-bellied dummy over a red-bellied dummy. Females showed no preferences when presented with i) an all-red and uniformly tan dummy and ii) two dummies that differed only in the location of red colouration (belly versus dorsum). In the three experiments in which females preferred a 25% red dummy, the proportion of courtship directed to this dummy increased with overall female responsiveness. The results of mathematical models of colour opponent and luminosity processing suggest that female preferences are influenced by a male's belly colour contrast and not by merely its brightness contrast.

Male Mating Preference in Sticklebacks: Effects of Repeated Testing and Own Attractiveness

In sticklebacks, Gasterosteus aculeatus, males have conspicuous nuptial coloration, whereas females are cryptically coloured. Usually females are the choosy sex in mate choice, but under certain conditions males may be choosy too. Females signal their spawning readiness, among others, by displaying a head-up courtship posture while pointing at the preferred male. We tested the male's preference for this posture by offering males a simultaneous choice of two stylized dummies of ripe females, one in head-up posture and one horizontal. The males directed relatively more courtship to the head-up dummy, and tended to do the more so the more intense the blue iris of their own eyes (corrected for differences in male length). Because the blue eye colour is a criterion of female choice in this population, attractive males tended to be choosier. Upon repeated presentation of the dummies to the same males on subsequent days, the malcs' preference for the head-up dummy disappeared, but there was no change in total courtship activity. When confronted with a different, more realistic pair of dummies, the same males showed again a preference for the head-up posture suggesting that male preference can be influenced by experience.

Video mate preferences of female three-spined sticklebacks from populations with divergent male coloration

This study evaluated whether diversity in male ornamental traits between populations is associated with a corresponding diversity in female preferences, or whether males can evolve divergent ornamentation even when female preferences remain relatively consistent. Video editing techniques were used to manipulate the coloration of recorded images of male three-spined sticklebacks, Gasterosteus aculeatus, and these images were presented to female sticklebacks from populations with black or red male nuptial coloration. Overall, females responded preferentially to images of males with black or red coloration over images with the dull coloration of females and some males; although preferences differed between populations, these differences were not statistically significant. Thus divergence in male ornaments was probably not caused by a corresponding divergence in female preferences. The results do not, however, allow clear discrimination between the various hypotheses for the evolution of female mating preferences.

Nuptial coloration in the sand lizard, Lacerta agilis: an intra-sexually selected cue to fighting ability

Abstract. In the sexually dichromatic sand lizard the area of the nuptial green coloration in males is allometrically related to body mass, and males with higher fighting ability have more saturated nuptial colours. Experiments in the laboratory showed that the extent of the bright nuptial coloration in males affects their contest behaviour; manipulated males with more colour were more likely both to initiate contests and to win. Further, when manipulated males had badges of unequal size the contests were settled more quickly than when the badges were the same size. This predicts that superior fighters with larger badges should have higher mating success; this was confirmed by field studies of a natural population.

Why are sand lizard males (Lacerta agilis) not equally green?

Sexual selection theory and game theory posit that cues to mate quality and fighting ability should be costly to be honest. Male sand lizards (Lacerta agilis) consider a rival's nuptial coloration when making strategic decisions in contests, and in this paper I examine five mechanisms (both proximate and ultimate ones) that could constrain male nuptial coloration. Three of these mechanisms were rejected as potential constraints on male nuptial coloration: testosterone, predation, and parasites. Two mechanisms could not be rejected as constraints on male pigmentation: differential allocation of energy to reproduction versus somatic growth among males, and social costs due to high aggression from conspecific males.

Sexual selection in an anadromous population of threespine sticklebacks ? no role for parasites

We examined the hypothesis that trematode parasites played a role in the evolution of the red colour of male threespine sticklebacks (Gasterosteus aculeatus L.) and whether the parasites affected female fitness. Parasites (‘blackspot’ disease) played no role either in determining the outcome of male—male competition for breeding territories or in female mate choice. Among males with territories, mating success was highly variable. Some males obtained over 3000 eggs (approximately 10 matings) whereas others received none. In 1 year of the 2 year study, males with the greatest amount of red nuptial coloration had the greatest mating success. Although male colour may sometimes affect female choice in this system, this preference has probably not evolved because of the Hamilton—Zuk mechanism of sexual selection. The parasites had small, but statistically significant effects on female fitness. Females with high parasite loads were in poorer condition and produced fewer eggs than less parasitized fish.

Nuptial coloration and predation risk in model sand lizards, Lacerta agilis

Animals in social aggregations use signals of quality or motivation to attract mates and intimidate rivals. Theory indicates that honesty can be maintained in these signals if the costs of signalling affect low-quality individuals more than they affect high-quality individuals. Considerable research has focused on identifying the nature of those costs and their ability to maintain honest signals. Much of this research, particularly in recent years, has focused on receiver-independent physiological costs of signal production. Less research attention has been paid to receiver-dependent costs that might arise from conspecific responses to signals. Here we survey the literature on these different types of costs, focusing in particular on case studies from a diversity of taxa. We find that signals often do carry significant physiological production costs, but this is not universal, as many signals appear to be physiologically inexpensive to produce. More importantly, very few studies have tested the key prediction that physiological production costs differentially affect low-quality individuals over high-quality individuals. In contrast, research from a diversity of taxa indicates that signals such as coloration and vocalizations often affect agonistic interactions, which in turn affect the production of signals, and that deceptive signallers receive more aggression than do honest signallers in at least some systems. Social costs are a plausible but understudied mechanism for maintaining honest signalling.

Temporal changes in the structure of the male nuptial signal in the brook stickleback, Culaea inconstans (Kirtland)

Within the Gasterosteidae, only members of the clade Culaea + Pungitius + Gasterosteus contain nuptially coloured males. Of these males, the nuptial signal has been subjected to detailed experimental examination in one species, the three-spined stickleback, Gasterosteus aculeatus. Since most components of the signal did not originate in G. aculeatus, descriptions of signal structure and variability for other members of the Gasterosteidae are a critical prerequisite to discussions of the processes underlying the evolution of male nuptial colouration in these fish. In this paper I investigated the changes in the male nuptial signal for another member of the clade, the brook stickleback, Culaea inconstans. The results of this investigation revealed that as in G. aculeatus, the signal is a complex mosaic, in this case representing the interaction between changes in the intensity of black pigmentation in the ventral – lateral body surface, the dorsal – lateral body surface, the eye bar, the fins, and the spines. These variables interacted to produce four distinct male colour mosaics corresponding to the stage a male had reached in the breeding cycle and the sex of an intruding conspecific.

The Breeding System of the Three-Spined Stickleback, Gasterosteus Aculeatus (Forma Leiura) With Reference To Spatial and Temporal Patterns of Nesting Activity

Abstract1) The breeding succes of three-spined stickleback (Gasterosteus aculeatus L., forma leiura) males in a small stream of the Tsuya River, Gifu Prefecture, Central Japan, was studied with reference to timing of nesting initiation, use of space for nesting and social interactions. The observations were made almost daily during March to early July 1988 along the shore at a distance of 1-2 m from the fish and nests. 2) All the males in an enclosed study pool were individually marked (99 males). Furthermore, a total of 67 females were marked and observed weekly. The males were individually observed and their agonistic, courtship and parental behaviour as well as their reproductive success were quantified. Reproductive success of individual male was measured as the number of nests built, the number of successful nests, the number of hatched fry per nest. Nest sites were categorized in six types (A-F) on the basis of the proportion of vegetation cover around the nest and distance from the shore. 3) Body size and environmental factors (water temperature, water depth, changes in water level) were not correlated with reproductive success. Flooding was not a major cause of unsuccessful nesting. The brightness of nuptial colouration at the onset of breeding correlated significantly with individual success. Individual variation in the development of secondary sexual characteristics such as a nuptial colouration may have an important consequence for the lifetime reproductive success of the individuals. There was no relationship between fish density and reproductive success. 4) All males that nested more than once had begun breeding early in the season. The sooner a male started nest-building, the more opportunities he had to complete breeding cycles. 5) After an unsuccessful nest, males were significantly more likely to move their nest sites than after a successful nest. The subsequent nesting cycle was not always successful. 6) There was variation in nest-sitc location. The spatial pattern of nest distribution was strongly related to the temporal pattern, because the first males which settled, more often built their nests at sites along the shore where the nest was covered on one or two sides by vegetation. The location of nest site was significantly correlated with reproductive success. When males nested in partly concealed places along the shore, they could sometimes obtain a high reproductive success irrespective of the date of breeding initiation. Thus, reproductive success was largely determined by the timing of nest-building and nest position.

INTEGRATING PHYLOGENY AND EXPERIMENTAL ETHOLOGY: FROM PATTERN TO PROCEs.

Phylogenetic systematics offers ethologists a method for uncovering macroevolutionary patterns of behavioral diversity, which can be used to generate predictions for experimental investigation of microevolutionary processes. I used phylogenetic methods to disentangle the contributions of various selection pressures in the evolution of sexually dimorphic nuptial coloration in gasterosteid fishes in general, and Gasterosteus aculeatus in particular. Based upon the phylogenetic relationships between breeding colors and breeding behaviors in the gasterosteids, three predictions relevant to a discussion of nuptial coloration in G. aculeatus were proposed. The origin and elaboration of nuptial coloration was (1) weakly associated with male/male interactions (intrasexual selection), (2) moderately associated with parental care (natural selection) and (3) strongly associated with male/female interactions (intersexual selection). I tested the hypothesized macroevolutionary relationships between male breeding color and behavior in two sets of experiments studying changes in male nuptial coloration across the breeding cycle and female choice based on intensity of male color. The results of these experiments at the microevolutionary level of analysis corroborated the macroevolutionary predictions and confirmed the original intuition of previous researchers: male body color intensity is an important component of female mate choice in G. aculeatus. This study demonstrates that a phylogenetic hypothesis can generate predictions that are experimentally testable and falsifiable.

Changes in plasma electrolyte and hormone concentrations during homing migration of chum salmon Oncorhynchus keta with special reference to the development of nuptial color.

Returning chum salmon Oncorhynchus keta captured by set-nets placed along the Shiretoko Peninsula Hokkaido contain both silvery and nuptial colored fish. The nuptial color further develops in spawning fish in the river. To clarify physiological changes during nuptial coloration, plasma osmolality, electrolite concentrations, and plasma levels of testosterone, estradiol-17β, growth hormone, thyroxine, and the thickness of the skin were investigated using the fish captured in September and October. Plasma osmolality and concentrations of sodium and chloride significantly decreased in the spawning group but there was no significant difference between the silvery and the nuptial colored groups. Plasma calcium and magnesium significantly decreased during nuptial coloration in both sexes. The thickness of the skin, especially the epidermis, closely correlated with the development of nuptial color. Plasma testosterone level also increased during nuptial coloration in both sexes, but the level of females captured in the sea was much lower than that of corresponding males. Plasma concentration of thyroxine of females captured in the sea was significantly lower than that of males. Growth hormone levels increased during nuptial colora-tion in both sexes, and stayed high even in the river. These results indicate that the nuptial colored salmon captured in the sea have the same adapting ability to the seawater as the silvery fish, and that testosterone might promote the nuptial coloration and thickening of the skin. Sexual differences of the testosterone levels detected in the seawater salmon suggest that other hormones, such as thyroxine, may act as an antagonist to testosterone.

Experimental investigations of the evolutionary significance of sexually dimorphic nuptial colouration in Gasterosteus aculeatus (L.): the relationship between male colour and female behaviour

Cladistic analysis of behavioural interactions during a series of female choice trials revealed three groups of reproductively unsuccessful males in a population of anadromous Gasterosteus aculeatus: inactive losers (losing male did not participate in choice test), active losers (losing male active during choice test), and fighting losers (subgroup of active losers defined by the observation that the female did not immediately follow the first male to approach her). The inactive losers group represents a "no choice" situation. In the remaining two groups, females responded preferentially to the most intensely coloured member of the competing male pair. This preferential response was strongest during the prechoice, captive presentation where the majority of females oriented head-up to, and tracked, the brighter red male. Once released, the female's initial response to the brighter courtship signal was overridden by the behavioural actions of the duller intensity male in 4 out of 12 trials. Although two of these males eventually lost the female to their rival, the remaining two individuals succeeded in spawning. Overall, 10 of 12 females spawned with the brighter red male. Given the brief breeding season and the advantage enjoyed by the most brightly coloured males in mate attraction, a high level of territorial intrusion is one way for an individual to attract a mate if he is surrounded by more intensely coloured neighbours.

Experimental investigations of the evolutionary significance of sexually dimorphic nuptial colouration in Gasterosteus aculeatus (L.): temporal changes in the structure of the male mosaic signal

Although classically described as "red," the three-spined stickleback male's nuptial signal is a complex mosaic of at least three colours: blue eyes, black dorsal–lateral body, and red ventral–lateral body. Seven variables (intensity, hue, and distribution of red body colour; intensity and hue of blue eye colour; intensity and distribution of black body colour) were scored for 19 males across an entire breeding cycle. These variables interacted to produce four distinct male colour mosaic signals corresponding with the stage a male had reached in the breeding cycle. No single variable was sufficient for the delineation of all breeding stages: however, the distribution of red body colour reliably distinguished the courting male from nesting and parental males. Variability in signal intensity between courting males was greatest for the red component of the nuptial signal and both intra- and inter-male variability in the overall intensity of red was greatest during courtship. Based upon these results, future investigations of the role of intersexual selection in shaping the male nuptial signal in this species should offer females a choice between males differing in the intensity of red rather than the traditional "red" versus "nonred" dichotomy.

Experimental investigations of the evolutionary significance of sexually dimorphic nuptial colouration in Gasterosteus aculeatus (L.): the relationship between male colour and male behaviour

The intensities of red body and blue eye colour in dull (and possibly bright) males reliably signals their behavioural vigour. Males with medium intensity colouration signal that they are more vigorous than their dull conspecifics; however, there is no association between colour and behavioural intensity within this group. A truth in advertising mechanism is thus potentially very powerful at either end of the colour intensity spectrum but is less effective for fish whose colouration is in the central section of the spectrum. Males with medium intensity colouration may be more strongly influenced by stochastic factors such as previous experiences or colour relative to neighbours. The increased importance of personal history introduces a source of disorganization into the mating system that may oppose the directional force of truth in advertising and thereby increase the ambiguity of the male colour signal.

LOSS OF NUPTIAL COLOR IN THREESPINE STICKLEBACKS (GASTEROSTEUS ACULEATUS).

Loss of conspicuous nuptial color in Gasterosteus aculeatus (threespine stickleback) has been reported from several localities in western North America and is ascribed to increased rates of predation or to convergent threat displays. I have examined 66 populations of G. aculeatus from the Queen Charlotte Archipelago and found extensive variation in the expression of red nuptial color. Males in 31 of the populations lack red throats, while males in five populations have major expression of red nuptial color. I test two hypotheses for nuptial-color loss: that the loss results from increased predation rates and that it involves differences in water spectra (relative transmission at 400 nm). Results, which are consistent with the second hypothesis, show that the greatest expression of red pigment occurs in habitats with the highest water clarity, while loss of red nuptial color is generally found in heavily stained waters. There is no correlation between nuptial-color loss and presence or absence of vertebrate predators. Two new hypotheses for these associations are proposed: signal-masking in spectrally restricted habitats and carotenoid deficiencies in the diet. Previous studies of red nuptial color and its loss in Gasterosteus merit additional attention, given the associations with underwater spectra.

Differences between the reproductive biologies of Tripterygion tripteronotus and T. delaisi (Pisces, Perciformes, Tripterygiidae): the adaptive significance of an alternative mating strategy and a red instead of a yellow nuptial colour

This paper contributes to the understanding of the evolution of alternative mating strategies by comparing morphological, ecological and ethological aspects of the reproductive systems of two closely related fish species studied near the marine biological station “STARESO” at Calvi, Corsica, between March 1982 and May 1985. The Mediterranean breeding areas of Tripterygion tripteronotus and T. delaisi partly overlap. The red territorial males of T. tripteronotus defend territories in the upper 6 m of the water column and the yellow territorial males of T. delaisi breed between a depth of 3 and 40 m. Small male T. tripteronotus possess relatively large gonads exhibit “sneaking” behaviour, while small male T. delaisi do not participate in mating. T. tripteronotus expends more effort in reproduction than T. delaisi. This is expressed in larger gonads, a higher density of and stronger competition for nest sites, and a longer breeding season and shorter spawning bouts with a higher fertilization rate in the former species. We hypothesize that the sneaking strategy of non-territorial male T. tripteronotus evolved in response to competition for nest sites in the shallow, upper water layers, which are limited in depth, but contain a good food supply. The depth restriction is imposed by the light-reflecting properties of the red territorial males. We suggest that the evolution of T. tripteronotus began with the appearance of a red morph of T. delaisi after the invasion of this latter species into the tideless Mediterranean Sea.

Loss of Nuptial Color in Threespine Sticklebacks (Gasterosteus aculeatus)

Loss of Nuptial Color in Threespine Sticklebacks (Gasterosteus aculeatus)